Zamia imbricata Calonje & J.Castro, 2021

Calonje, Michael, Hernández, Jonatan Castro, Coca, Luis Fernando, Jaramillo, Daniel & Aristizábal, Arturo, 2021, Two new species of Zamia (Zamiaceae, Cycadales) from the Magdalena-Urabá moist forests ecoregion of northern Colombia, Phytotaxa 497 (1), pp. 1-19 : 5-9

Zamia imbricata Calonje & J.Castro sp. nov. (Figs. 3A–E, 4A–J, 5A–G)

Diagnosis: —Distinguished within the genus by its subterranean stem, its petioles which are typically unarmed or rarely armed with minute scattered prickles, its rachis which is straight and horizontally disposed bearing highly imbricate leaflets held in a planar disposition, its leaflets which are lanceolate, papyraceous, and diminutive (3.9–11.6 × 1.2–1.9 cm) with strongly toothed margins, and its strobili which are held on extremely long peduncles (20+ cm) and which bear relatively flat and unornamented sporophylls.

Type: — COLOMBIA. Caldas: La Dorada, 244 m, 17 Feb 2020, J . Castro, M . Calonje, L. F . Coca & D. Jaramillo 1601 (holotype HUA!, isotype FAUC!) .

Additional specimens examined (paratypes): — COLOMBIA. Caldas: La Dorada: 200–245 m, 17 Feb 2020, J . Castro, M . Calonje, L. F . Coca & D. Jaramillo 1594 ( FMB!), 1595 ( COL!), 1602 ( HUA!), 9 Mar 2019, L. F . Coca & D. Jaramillo 13012 ( FAUC!), 17 Dec 2018, S. H . Gómez et al. SHG 3628 ( HUA!), 21 Dic 2018, D. Sanín et al. 7251 ( FAUC!, CUVC!) .

Description: — Stem hypogeous, typically solitary, cylindrical, 10–30 × 1–15 cm. Cataphylls caducous, chartaceous, triangular to narrowly triangular, 3.2–5.2 cm long and 1.0– 2.3 cm wide at the base, tan tomentose with cream-colored base, losing tomentum and base turning brown at maturity. Leaves 1–5 per apex, 13–200 cm long (58+ cm on adults), 10–19 cm wide, covered with white to beige tomentum at emergence and becoming glabrous at maturity, petiole erect to slightly spreading to 45° from the stem apex, rachis relatively straight and horizontally disposed in older leaves. Petiole 14–141 cm long (34+ cm on adults), ochre to olive green, typically unarmed but rarely with a few translucent scattered minute prickles 0.5–0.8 mm long, abruptly swollen base to 15 mm wide. Rachis 20–73 cm long (24+ cm on adults), ochre to olive green, unarmed. Leaflets 6–110 (40+ on adults), suboppositely to subalternately arranged, strongly imbricate, succubously or incubously arranged and forming a mostly planar leaf surface, with a pinna-to-pinna angle (pp-angle sensu Grobbelaar 2002: 23) of approximately 180° throughout most of the leaf except for the basalmost pair which have a pp-angle of approximately 120°, articulate insertion on rachis 3.6–4.8 mm wide, spaced 1.2–1.4 cm at leaf center, membranaceous, lanceolate, acute distally, symmetrical to slightly falcate, discolorous, dark green and dull to semi-glossy adaxially, light green and dull abaxially with 13–18 veins visible, margins revolute and bearing 5–25 marginal teeth 1.0– 2.5 mm long restricted to distal half, basal leaflets 4.0– 8.7 cm × 1.2–1.9 cm, middle leaflets 4.9–11.6 × 1.5–1.8 cm, apical leaflets 3.9–6.3 cm × 1.2–1.7 cm. Eophylls to 16.2 cm long, petiole 14.0 cm, rachis 2.2 cm, carrying 6 leaflets 45–48 × 13.4–14.4 mm. Pollen strobili 1–2, light reddish-brown, conical-cylindrical, at pollen shedding 2.8–3.0 × 0.7–0.8 cm, sterile apex obtuse and 2.0– 2.2 mm long, strobilar axis glabrous, peduncle olive brown and lightly covered with villous white tomentum, 20–25 × 0.30–0.35 cm. Microsporophylls spirally arranged in 6 orthostichies of 9–11 sporophylls each, obtrullate, 6.0–6.2 × 6.2–6.5 mm at pollen shedding, distal shield rounded and encompassing 30–50 % of microsporophyll length, hexagonal, external face light orange-brown tomentose, 3.0–4.0 mm tall × 3.0– 4.2 mm wide, abaxial surface of microsporophyll with 9–11 microsporangia aggregated into a single group along margins and extending beyond surface of lamina, adaxial surface glabrous and lacking microsporangia. Ovulate strobili 5.2–8.8 × 2.8–4.0 cm, solitary, reddish-brown to brown, cylindrical with short acute apex 20–40 mm long. Strobilar axes and megasporophyll pedicels glabrous on mature strobili, peduncle 25.0–31.5 × 0.60 to 0.75 cm, olive green with short white tomentum at maturity. Megasporophylls spirally arranged in 4 to 5 orthostichies of 5 to 6 sporophylls each, pedicel 8–10 mm long, sterile shield flat (not extruded), 5–6 mm thick with oblong-hexagonal distal face 9–13 mm tall and 18–22 mm wide and terminal face shallowly depressed. Seeds ovoid, at maturity 13.0–13.6 × 9.2–9.6 mm with orange-red sarcotesta 0.4–1.1 mm thick, sclerotesta 12.2–12.3 × 7.7–7.9 mm.

Etymology: —From the Latin ‘imbricatus’ meaning ‘covered with tiles’, referring to the strongly overlapping leaflets.

Distribution, habitat and climate: —The species occurs on steep slopes in tropical moist forest at an elevational range of 200– 245 m. The soils are sandy and well drained, with abundant organic material and leaf litter. The pH in the region is acid (4.5–5.0) and the soils are high in aluminum, iron, and manganese, and low in phosphorus, calcium, potassium, and sodium ( Ramírez Guapacha & Bohórquez Osorio 2013). The canopy ranges from 9–35 m with a partially open understory with moderate solar exposure. The most species-rich plant families in the region are Rubiaceae , Fabaceae , Araceae , Piperaceae , and Melastomataceae ( Ramírez Guapacha & Bohórquez Osorio 2013) .

The climate within the area of occupancy of Zamia imbricata is classified as tropical rainforest (Af) by the Koppen-Geiger classification system ( Geiger 1954, Köppen 1918, Kottek et al. 2006). The tropical rainforest climate is hot, humid, and wet, with no pronounced dry season. The annual mean temperature within the area of occupancy is

FIGURE. Vegetative characteristics of Zamia imbricata . A. Leaf. B. Median leaflet, adaxial side. C. Immature, expanding leaflet D. Adult plant with ovulate strobilus. E. Cataphyll. Photographs from type locality, illustration by Michael Calonje.

FIGURE. Reproductive characteristics of Zamia imbricata . A. Microsporophyll adaxial side. B. Microsporophyll abaxial side. C. Pollen strobilus cross-section, abaxial side. D. Pollen strobilus near pollen dehiscence. E. Pollen strobilus with characteristically long peduncle. F. Ovulate strobilus, near maturity. G. Mature seed with ripe sarcotesta. H. Mature seed sclerotesta. I. Megasporophyll with mature seed and unpollinated ovule, abaxial side. J. Ovulate strobilus with peduncle, near maturity. Photographs from type locality, illustration by Michael Calonje.

FIGURE. Zamia imbricata in habitat. A. Adult plant, with Michael Calonje. B. Distal leaflets, adaxial side. C. Distal leaflets, abaxial side. D. Close-up of unarmed petioles. The petiole on the left is newly emergent and still covered with tomentum. E. Adult microsporangiate plant, showing horizontal disposition of rachis and leaflets. F. Median leaflets showing imbrication with alternate succubous and incubous orientation. G. Immature leaflets in the process of expanding. Photographs A–C by Jonatan Castro, D–G by Michael Calonje.

27° C and the annual precipitation 2500 mm. The rainfall pattern is bimodal, with peaks in rainfall ocurring in April and October, and troughs ocurring in January and July. The driest month is January, with 50 mm of rain and the wettest month is October, with 314 mm.

Ecology:— The species occurs in sympatry with Zamia incognita , but no evidence of hybridization was detected, as all individuals observed of both species were morphologically consistent with no intermediate forms observed. While the pollination of Zamia incognita has been studied in great detail and its pollinators have been identified as beetles belonging to the genus Pharaxonotha Reitter ( Valencia-Montoya et al. 2017) , the pollinating agent of Z. imbricata has not been determined and it is unclear whether differences in pollinating agents could be one of the reasons for the apparent lack of hybridization between the two species. Other possible reasons include sexual incompatibility between the two species since Z. incognita does not belong in the manicata clade (Calonje et al. 2017), or differences in their reproductive phenology. Unfortunately, the phenology for Z. imbricata remains largely unknown and will require additional field studies to better understand. Pollen cones approximately 1 to 2 weeks from pollen release were observed in mid-February of 2020 as well as near mature, mostly unpollinated ovulate cones. A single full-sized seed with a fully formed sclerotesta and a light pink sarcotesta was found in an ovulate cone and fully matured in the excised cone two months later. Other biological interactions involving Z. imbricata also remain unrevealed. A few leaves were observed with damage consistent with herbivory, but no insects were observed feeding on the leaves.

Conservation: —The species is known from a single location within a forest fragment of approximately 1 km 2 in La Dorada municipality of Caldas. Despite occurring in a healthy forest fragment, the plant was very rare at the surveyed location, with only 15 plants observed after four days of vigorous searching, and no live seedlings observed, only the remains of a single recently deceased seedling. Seed set was extremely poor, with only a single pollinated ovule observed in two separate seed cones. The above suggests that there are too few and/or too widely separated individuals to sustain a healthy population, and that no seedling recruitment is occurring at its only known location. Based on the above, we recommend this species be listed as Critically Endangered (CR) based on IUCN Red List criteria B1ab(iii,v)+2ab(iii,v); C2a(i,ii); D (IUCN Standards and Petitions Sub-committee, 2017).

Morphological and taxonomic affinities: — Z. imbricata appears most closely related to the currently undescribed species of Zamia “Cogollo” (Fig. 6). The two species are the southernmost species of the manicata clade and occur in the Magdalena River valley along the eastern foothills of the Cordillera Central, approximately 75 km distant from each other (Fig. 2). Both have small membranaceous leaflets and petioles that are unarmed or rarely with minute scattered prickles, but the species can readily be distinguished based on qualitative characters (Table 1). The leaflets of Z. imbricata are lanceolate (length-to-width ratio <7:1), imbricate, and flatter than those of Zamia . “Cogollo” which are linear-lanceolate (length-to-width ratio> 7:1), not imbricate, and with a distinct adaxially raised longitudinal crease. Furthermore, Z. imbricata generally attains smaller dimensions with shorter leaf length (to 2.0 m vs. 2.5 m) and shorter leaflet length (to 10 cm vs. 25 cm). Lastly, the sterile cone apex in ovulate strobili of Z. imbricata are shorter, typically less than 1 cm long vs. those of Zamia “Cogollo” which typically exceed 1.5 cm. The short, broad, membranaceous leaflets of Z. imbricata somewhat resemble those of the Mexican species Z. vazquezii D.W.Stev., Sabato & De Luca in Stevenson et al. (1998: 14). However, the leaflets of Z. vazquezii are not held in a planar disposition as they are in Z. imbricata , the peduncles are much shorter (<10 cm vs.> 15 cm), and the microsporophylls bear more numerous microsporangia (18–22 vs. 9–11).